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Received: 18 September 2018    Revised: 24 February 2019    Accepted: 26 February 2019

DOI: 10.1002/ece3.5086

ORIGINAL RESEARCH

Quaternary climatic fluctuations and resulting climatically

suitable areas for Eurasian owlets

Pankaj Koparde1,2,3  | Prachi Mehta4  | Shomita Mukherjee1*  | V. V. Robin3*

1
Division of Conservation Biology, Sálim Ali
Centre for Ornithology and Natural History,
Coimbatore, India
2
Manipal Academy of Higher Education,
Manipal, India
3
Indian Institute of Science Education and
Research (IISER), Tirupati, India
4
Wildlife Research and Conservation
Society, Pune, India
Correspondence
Pankaj Koparde, Division of Conservation
Biology, Sálim Ali Centre for Ornithology
and Natural History, Coimbatore, Tamil
Nadu, India.
Email: pankajkoparde@gmail.com
Funding information
Ministry of Environment, Forest and
Climate Change, Grant/Award Number:
J.22012/61/2009-CS (W); Indian Institute
of Science Education and Research Tirupati;
Department of Biotechnology, Government
of India, Grant/Award Number: BT/PR4812/
BCE/8/898/2012
Abstract
Aim: The nested pattern in the geographical distribution of three Indian owlets, re-
sulting in a gradient of endemicity, is hypothesized to be an impact of historical cli-
mate change. In current time, the Forest Owlet Athene blewitti is endemic to central
India, and its range is encompassed within the ranges of the Jungle Owlet Glaucidium
radiatum (distributed through South Asia) and Spotted Owlet Athene brama (distrib-
uted through Iran, South and Southeast Asia). Another phylogenetically close spe-
cies, Little Owl Athene noctua, which is largely Palearctic in distribution, is hypothesized
to have undergone severe range reduction during the Last Glacial Maximum, showing
a postglacial expansion. The present study tests hypotheses on the possible role of
Quaternary climatic fluctuations in shaping geographical ranges of owlets.
Methods: We used primary field observations, open access data, and climatic niche
modeling to construct climatic niches of four owlets for four periods, the Last
Interglacial (~120–140 Ka), Last Glacial Maximum (~22 Ka), Mid‐Holocene (~6 Ka),
and Current (1960–1990). We performed climatic niche extent, breadth, and overlap
analyses and tested if climatically suitable areas for owlets are nested in a relatively
stable climate.
Results: Climatically suitable areas for all owlets examined underwent cycles of ex-
pansion and reduction or a gradual expansion or reduction since the Last Interglacial.
The Indian owlets show significant climatic niche overlap in the current period.
Climatically suitable areas for Little Owl shifted southwards during the Last Glacial
Maximum and expanded northwards in the postglaciation period. For each owlet, the
modeled climatic niches were nested in climatically stable areas.
Main Conclusions: The study highlights the impact of Quaternary climate change in
shaping the present distribution of owlets. This is relevant to the current scenario of
climate change and global warming and can help inform conservation strategies, es-
pecially for the extremely range‐restricted Forest Owlet.

*Equal contribution.

This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium,
provided the original work is properly cited.
© 2019 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.

Ecology and Evolution. 2019;1–11. www.ecolevol.org |  1

  
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2       KOPARDE et al.
KEYWORDS
citizen science, comparative biogeography, Forest Owlet, geographical range, last glacial
maximum, little owl, quaternary climatic fluctuations
1 |  I NTRO D U C TI O N
Past climatic fluctuations have played a major role in shaping the
ranges of several species, especially endemic and endangered spe-
cies in the regions harboring much of today's biodiversity such as
the tropics (Bose, Munoz, Ramesh, & Pélissier, 2016; Bueno et al.,
2017; Carnaval & Moritz, 2008; Costa et al., 2018; Pinilla‐Buitrago,
Escalante, Gutiérrez‐Velázquez, Reyes‐Castillo, & Rojas‐Soto, 2018;
Werneck, Nogueira, Colli, Sites, & Costa, 2012). Regions that ex-
perience low climatic variation (climatically stable) are believed to
have more endemic species (Dynesius & Jansson, 2000). Jansson
(2003) proposed that Milankovitch cycles during the Quaternary
are responsible for current global geographical patterns of endemic
species. The effect of the Last Interglacial (LIG: ~120 –140 Ka), Last
Glacial Maximum (LGM: ~18–22 Ka), and Mid‐Holocene (MDH:
~6 Ka) seems to be very prominent for several taxa (Jansson, 2003;
Ramachandran, Robin, Tamma, & Ramakrishnan, 2017). Here, both
the LIG and LGM periods represent periods of extreme climatic
conditions.
During the LIG, temperatures warmer than the pre‐industrial
Holocene climate prevailed globally (reviewed in Kukla et al., 2002;
Otto‐Bliesner, Marshall, Overpeck, Miller, & Hu, 2006), with tropi-
cal areas exhibiting robust monsoonal systems (Pedersen, Langen, &
Vinther, 2017). The LGM was the most recent driest period on Earth.
The LGM characterized low average temperature, increased aridity,
and a drop in sea levels (Clark & Huybers, 2009), leading to a change
in climate, available land area, and climate‐associated changes in veg-
etation (Anhuf et al., 2006; Bose et al., 2016). These changes possi-
bly altered the ranges of many species. In the Holocene (~11.7 Ka to
Present), a warmer climate than the LGM prevailed in the Northern
Hemisphere but the tropics were colder than the present (Mayewski
et al., 2004; Steig, 1999; Wanner et al., 2008).
Knowledge from the Quaternary period suggests that species
responses to past climate change can provide crucial information
on their current and future evolutionary and ecological trajectories.
Birds are among the most widely studied taxa with respect to cli-
mate change effects. Studies have shown a drastic negative impact
of climate change on bird distributions (Hilbert, Bradford, Parker,
& Westcott, 2004; Ramachandran et al., 2017; Smith, Gregory,
Anderson, & Thomas, 2013) and demography (Howard et al., 2018;
Tomotani et al., 2018; Zhao et al., 2012), in many cases compromis-
ing their persistence (Crick, 2004; Urban, 2015).
In this paper, we examine the effect of the Quaternary climatic
fluctuations on the climatic niche extents of owlets that show a gra-
dient of endemicity and overlap in their current geographical dis-
tributions in parts of their ranges. Such comparative biogeography
studies are scarce and have been recommended to comprehend
community responses to global climate change (Berg et al., 2010).
Six species of owlets are known from India, of which Jungle Owlet
Glaucidium radiatum (Temminck), Spotted Owlet Athene brama
(Temminck), and the highly range‐restricted and Endangered Forest
Owlet Athene blewitti (Hume) (BirdLife International, 2017) are sym-
patric in central India. The Little Owl Athene noctua (Scopoli) of
Palearctic region partially overlaps in distribution with the Spotted
Owlet. The four owlets with varying range extents, habitat require-
ments and degrees of overlap with each other are phylogenetically
closely related (Koparde et al., 2018). Understanding how their
ecological and evolutionary histories shaped their current distribu-
tion can provide vital information on how they respond to climatic
changes, which will help plan their conservation strategies in the
current scenario, especially in case of the Endangered Forest Owlet.
Divergence estimates from the phylogeny of Indian owlets in-
dicate that the Plio‐Pleistocene climate change may have played an
important role in the speciation of Athene and Glaucidium owlets
(Koparde et al., 2018) that could explain patterns of their current
ranges. Pellegrino et al., (2014), suggest that the Little Owl sur-
vived in the European Southern Refugia (Iberian, Italian, and Balkan
Peninsula) during the LGM, when much of its distributional range
was covered in ice, and later expanded into its current range.
In the present study, we explore if Quaternary climatic fluctua-
tions played a role in shaping the geographical distributions of owl-
ets, using past‐projected climatic niche models (CNMs) and examine
if the suitable areas for the endemic and Endangered Forest Owlet
were nested within climatically stable areas to a greater extent, as
compared to the other relatively widespread species.
2 | M E TH O DS
2.1 | Target species
The four target species are the Forest Owlet, Jungle Owlet, Spotted
Owlet, and Little Owl and are presented in Figure 1. The Forest
Owlet has a narrow and severely fragmented range across central
India with an Extent of Occurrence (EOO) of 55,300 km2 (Birdlife
International, 2017) and hence is a priority species in conserva-
tion. The Jungle Owlet occurs across Peninsular India and Sri Lanka
(EOO = 3,470,000 km2) (Birdlife International, 2016a). The Spotted
Owlet is distributed across most of the Indian Subcontinent, from
Iran to the West to Myanmar in the East and from the Himalayas
in the North to the Southern tip of India, except in Sri Lanka
(EOO = 10,800,000 km2) (Birdlife International, 2016b). The three
owlets (henceforth referred as “Indian owlets”) show a gradient of
KOPARDE et al.
F I G U R E 1   The study owlets and their present distribution provided by Birdlife International (2016a, 2016b, 2016c, 2017). Red regions
indicate the geographical distribution of species. Photo credits: Forest Owlet by PM, Spotted Owlet and Jungle Owlet by Chinmay Rahane,
and Little Owl by Snehasis Sinha
endemicity and a nested pattern in the extent of their geographic
ranges. The Little Owl, sister to Spotted Owlet, mainly distributed
in the Palearctic (EOO = 52,900,000 km2) (Birdlife International,
2016c), also occurs in the Indian Himalayas, partially overlapping
in geographical distribution with the Spotted Owlet. Since the owl-
ets are of similar size (20–24 cm) (Ali & Ripley, 1983; Rasmussen &
Collar, 1998) and Forest Owlet distribution overlaps completely with
Spotted Owlet and Jungle Owlet distributions in central India, they
can be potential competitors in areas of sympatry (Ishtiaq, 2000;
Jathar & Rahmani, 2004; Mehta, Kulkarni, Talmale, & Chandarana,
2018; Rasmussen & Ishtiaq, 1999). At a finer scale, however, their
habitat associations are reported to be different. The Spotted Owlet
and Little Owl are associated with open habitats and considered to
be synanthropic while the Jungle Owlet is associated with dry to
moist deciduous open forests and scrublands (Ali & Ripley, 1983).
The Forest Owlet is restricted to the Teak dominated dry decidu-
ous forests of central India (Mehta, Kulkarni, Mukherjee, Chavan, &
Anand, 2017; Mehta, Kulkarni, Patil, Kolte, & Khatavkar, 2008).
We obtained Forest Owlet locations from published literature
(n = 30) (Chavan & Rithe, 2009; Ishtiaq & Rahmani, 2000,2005;
Jathar & Rahmani, 2004; Kasambe, Pande, Wadatkar, & Pawashe,
2004; King & Rasmussen, 1998; Laad & Dagale, 2014; Patel et al.,
2015) and primary field observations (n = 25). We filtered the ini-
tial dataset of 55 points to 50 points, avoiding spatially overlapping
points. We did not use citizen science based portals for collecting
Forest Owlet location data, due to uncertainty associated with
these reports and the accuracy of location coordinates. For other
owlets, we collected presence locations from eBird (eBird, 2017;
Sullivan et al., 2009) and iNaturalist (iNaturalist, 2017). The eBird
and iNaturalist observations were filtered to restrict the duration
to the years from 1970 to 2016 and include coordinate certainty
below 2 km. We curated the point locations for all other owlets and
filtered them by country (excluding countries where the species is
introduced or traded), date (including records from 1970 to 2016),
|
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area (including GPS coordinate certainty below 2 km), and approved
and reviewed status. We retrieved a total of 23,243 and 202 points
for Little Owl from eBird and iNaturalist, respectively. By using the
country filter, points from New Zealand were avoided, where the
species has been introduced recently. Finally, 2,438 and 84 points
(total n = 2,522) were retained from eBird and iNaturalist, respec-
tively. Similarly, we filtered 18,472 eBird and 73 iNaturalist records
of Spotted Owlet to a final count of 6,042 eBird and 27 iNaturalist
records (total n = 6,069). For Jungle Owlet, we filtered 3,962 eBird
and 20 iNaturalist records to a final count of 2,743 eBird and 15
iNaturalist records (total n = 2,758).
2.2 | Data collection—climate data
We extracted the climate dataset available for four time peri-
ods, LIG (~120–140 Ka), LGM (~22 Ka), MDH (~6 Ka), and cur-
rent (1960–1990) from <http://www.worldclim.org/> (Hijmans,
Cameron, Parra, Jones, & Jarvis, 2005). Datasets for the LGM,
MDH, and current time period were available at 2.5′ (around
5 km2); this being the highest resolution for the LGM and MDH
datasets. The available dataset for the LIG was 30″ (around 1 km2)
resolution (Otto‐Bliesner et al., 2006). Therefore, we scaled the
LIG dataset to 2.5′. We used the LGM and MDH dataset from the
Community Climate System Model (CCSM4) (Gent et al., 2011)
following Fuentes‐Hurtado, Hof, and Jansson (2016). We clipped
raster files of the bioclimatic variables at two extents to be used
in the analysis, the Indian Subcontinent for the Indian owlets re-
stricted to the Indian Subcontinent (5 N to 39.1 N and 55.1 E to
109.9 E) and Eurasia and parts of North Africa for Little Owl (0.71
N to 63.62 N and −20.08 E to 134.46 E). The geographical extent
under modeling is a crucial factor in determining the accuracy of
species distribution models (Barve et al., 2011; VanDerWal, Shoo,
Graham, & Williams, 2009). Therefore, we used two different ex-
tents to capture the predictor range better.
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4       KOPARDE et al.

TA B L E 1   Summary of the best‐fit

Species Variables used Training AUC Test AUC
climatic niche models (CNMs) for the
Forest Owlet BIO2, BIO5, BIO6, BIO9, BIO10, BIO11, 0.996 0.994 current time period. Variables used are
BIO15, BIO18 the same as for the past‐projections
Spotted Owlet BIO3, BIO6, BIO7, BIO11, BIO12, BIO13, BIO15 0.879 0.876
Jungle Owlet BIO2, BIO3, BIO4, BIO10, BIO11, BIO12, 0.951 0.949
BIO13, BIO15
Little Owl BIO1, BIO5, BIO10, BIO11, BIO14, BIO18, 0.926 0.924
BIO19

Note. BIO1, Mean annual temperature; BIO2, Mean diurnal range; BIO3, Isothermality; BIO4,
Temperature seasonality; BIO5, Maximum temperature of warmest month; BIO6, Minimum tem-
perature of coldest month; BIO7, Temperature annual range; BIO9, Mean temperature of driest
quarter; BIO10, Mean temperature of warmest quarter; BIO11, Mean temperature of coldest quar-
ter; BIO12, Annual precipitation; BIO13, Precipitation of wettest month; BIO14, Precipitation of
driest month; BIO15, Precipitation seasonality; BIO18, Precipitation of warmest quarter; BIO19,
Precipitation of coldest quarter.

other CNM approaches, we assume that current species–climate re-

2.3 | Climatic niche models
We created bias files for all owlets to correct for sampling bias in
modeling (Kramer‐Schadt et al., 2013). We used MaxEnt v 3.4.1
(Phillips, Anderson, & Schapire, 2006) for CNMs. We performed all
the Pre‐ and Post‐MaxEnt data analyses in ArcGIS v10.1 (ESRI, 2011)
and SDMToolbox (Brown, 2014) in ArcGIS. For CNMs, we followed
Fuentes‐Hurtado et al. (2016) modeling protocol with modifications.
We first performed a correlation analysis on all 19 bioclimatic predic-
tors for the current time period to detect highly correlated (r > 0.8,
r < −0.8) variables. To select the appropriate variables from pairs of
highly correlated ones, all 19 variables were used in a MaxEnt run
(replicate type = bootstraps, replicate runs = 50) and variables that
contributed maximally in jackknifing runs were noted. For further
analysis, we retained only those variables (from a correlated pair)
that had high contributions in the MaxEnt output and were impor-
tant considering the natural history of each owlet. This procedure
has been used elsewhere (Carroll, 2010; Peterson & Robins, 2003).
The selected variables for each species are shown in Table 1. We
followed this procedure to fine‐tune the models and avoid overfit-
ting (Lee‐Yaw et al., 2016; Radosavljevic & Anderson, 2014). The
final MaxEnt models were run with 50 bootstrap iterations. We set
the regularization parameter to 1.5 to avoid overfitting of data. To
determine the robustness of the model in terms of Test and Training
AUC values, we randomly picked 25% of points as test points. We
performed backward‐time simulations by projecting CNM for the
current period for each owlet at three time periods, MDH, LGM, and
LIG. We used a 10th percentile logistic training presence threshold
to convert continuous raster maps into binary maps to better visual-
ize the change in the extent of climatic niche. The 10th percentile
logistic threshold is a conservative estimator of predicted climatic
niches and has been applied to avoid overfitting of models (Kumar
& Stohlgren, 2009; Pearson, Raxworthy, Nakamura, & Townsend
Peterson, 2007). The fossil data available on the study owls are
scanty, mainly available for the Little Owl from Europe (Bedetti &
Pavia, 2013; Mlikovsky, 2002; Pavia, Manegold, & Haarhoff, 2014);
hence, validation of the past CNMs was not possible. Here, as with
lationships have been maintained in the past.
2.4 | Post‐CNM analysis
We performed intersection and stability analyses on climatically suit-
able areas by superimposing suitable area polygons for a specific time
period with another time period. We treated areas common to both the
polygons (intersection analysis) as conserved areas (niche stable) and
nonoverlapping areas as shift (contraction/expansion/displacement) in
the climatic niche. We performed niche overlap analysis to compute
I statistic (Warren, Glor, & Turelli, 2008) and niche breadth analysis
to compute the B2 statistic (uncertainty index) (Nakazato, Warren, &
Moyle, 2010) using ENMTools v1.4.4 (Warren, Glor, & Turelli, 2010)
to explore niche overlap across time periods and species. The niche
overlap index (I statistic) varies between 0 (no overlap) and 1 (com-
plete overlap). The higher values in case of B2 index represent broader
niche. Finally, we created a climatic heterogeneity layer for each time
period using SDMToolbox in ArcGIS. The climatic heterogeneity in-
formation is in percentage (0–100), 0 signifying highly homogenous
(stable) climate and a value of 100 indicating highly heterogeneous
climate. Climatic heterogeneity information was extracted based on
1,000 random points generated for each suitable area polygon to test
if the predicted climatically suitable areas of owlets fall in areas with
higher climatic stability, expecting that suitable areas for the endemic
Forest Owlet will be nested in climatically stable zones as compared to
the widespread owlets. We performed one‐way ANOVA test on the
climatic heterogeneity data to test for variation within a species across
time periods and between species for each time period.
3 | R E S U LT S
3.1 | Climatically suitable areas and niche breadth of
owlets
The models had a low false positive rate (model summaries
in Table 1). Climatically suitable areas for the Forest Owlet
KOPARDE et al. |
      5

F I G U R E 2   Binary maps of climatically suitable areas suggest that Quaternary climatic fluctuations affected all owlets differently. The red
and gray colors indicate suitable and unsuitable areas, respectively. (a–d) The Forest Owlet maps; (e–h) The Spotted Owlet maps; (i–l) The
Jungle Owlet maps; and (m–p) The Little Owl maps. The map of climatically suitable areas of the Little Owl is clipped to match the modeling
extent used for other owlets for a comparative purpose

underwent a cyclic reduction and expansion throughout the
four time periods (Figure 2a–d, Table 2, Supporting Information
Appendix S1: Figure S1.1.), with the maximum niche breadth and
extent of suitable areas attained during the LIG and minimal dur-
ing current time period. The suitable areas for the Forest Owlet
in central India and the northern Western Ghats appeared to be
conserved across time (Supporting Information Appendix S1:
Figure S1.1.). Results for the Spotted Owlet indicate that climati-
cally suitable areas for the species underwent expansion during
the LGM and progressive reduction in MDH and current time
periods (Figure 2e–h, Table 2, Supporting Information Appendix
S1: Figure S1.2.). Climatically suitable areas for the Jungle Owlet
showed a progressive expansion post‐LIG up to the current time
period (Figure 2i–l, Table 2, Supporting Information Appendix S1:
Figure S1.3.). Post‐LIG, during the LGM period climatically suita-
ble areas for the Little Owl, reduced, but progressively expanded
post‐LGM up to the current time period (Figure 2m–p, Table 2,
Supporting Information Appendix S1: Figures S1.4. and S1.5.).
We detected a southward shift during the LGM and northward
expansion post‐LGM in climatically suitable areas for the Little
Owl (Figure 2m, Table 2, Supporting Information Appendix S1:
Figure S1.5.).
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6       KOPARDE et al.

TA B L E 2   Climatically suitable areas and niche breadth for expansion; whereas suitable areas for other currently widespread
owlets across four time periods owlets showed either an overall progressive expansion or reduc-

Niche Breadth tion (Figure 2, Table 2). The change in climatically suitable areas for
Species Time period Extent (km2) – B2 (*100) the Indian owlets might be a function of climate and climate‐me-
diated change in habitat, prey, and interactions among these spe-
Forest Owlet Current 21,197 82.69
cies. Currently, the Forest Owlet is sympatric with Jungle Owlet and
MDH 486,051 93.4
Spotted Owlet whereas the Jungle Owlet and Spotted Owlet over-
LGM 140,794 93.62
lap in occurrence in parts of their overall distributional ranges.
LIG 1,261,067 94.76
The niche breadth and extent of climatically suitable areas for
Spotted Owlet Current 941,649 93.55
the Forest Owlet were at its maximum in the LIG (Table 2), which
MDH 1,474,825 94 was wetter and warmer than the pre‐industrial Holocene. During
LGM 1,714,729 94.58 this time period, other Indian owlets had relatively constricted cli-
LIG 812,163 93.14 matically suitable areas in the Indian Subcontinent. During the LIG,
Jungle Owlet Current 260,700 90.50 Jungle Owlet which is currently associated with forest and scru-
MDH 6,297 85.37 bland habitats and has a relatively younger divergence (1.8–0.1 Ma,
LGM 2,425 85.67 Koparde et al., 2018), might have survived in the pockets of the
LIG 478 85.51 south Western Ghats, especially in the eastern parts of the Western

Little Owl Current 1,781,868 92.72
MDH 289,030 82.1
LGM 301,570 79.12
LIG 360,646 78.54
Note. B2: Niche breadth in the range of 0 to 1 (low to high).
3.2 | Climatic heterogeneity and niche overlap
We detected overlap (I = 0.62–0.98) in climatic niche of the Forest
Owlet across the four time periods (Supporting Information
Appendix S2: Table S2.1.). A similar pattern was seen for the Jungle
Owlet (I = 0.59–0.86) and Spotted Owlet (I = 0.94–0.98). For the
Little Owl, niche overlap was the least (I = 0.29–0.59) across the four
time periods. When comparing overlap in niche between pairs of
species for each time period, high overlap was observed between
the Forest Owlet and Spotted Owlet (I > 0.9), except for the cur-
rent time period (I = 0.66). The Spotted Owlet, Jungle Owlet, and
Little Owl showed high niche overlap only in the current time period
(I > 0.8). The modeled climatically suitable areas of all the owlets
were nested in climatically stable areas throughout the four time pe-
riods (Figures 3 and 4, Supporting Information Appendix S1: Figures
S1.6. and S1.7., Appendix S2: Table S2.2.). In the current time period,
all owlets occupied areas with higher climatic stability than in the
past.
4 |  D I S CU S S I O N
4.1 | Quaternary climatic fluctuations and
climatically suitable areas for owlets
Assuming that the owlets have tracked the climatically suitable
areas predicted by our models, we detected variable responses of
the four owlets to the Quaternary climatic fluctuations. The cli-
matically suitable areas for the currently severely range‐restricted
Endangered Forest Owlet showed distinct cycles of reduction and
Ghats (Figure 2). Considering the LIG scenario (Figure 2), it appears
that Jungle Owlet had an insignificant presence in Peninsular India
and hence would have played a negligible role as a possible compet-
itor to other Indian owlets at this time. Little Owl was widespread
across the Palearctic in LIG and occupied relatively northward areas
as compared to its climatically suitable areas during the LGM.
During the LGM, climatically suitable areas for the Forest Owlet
showed a drastic reduction while for the Spotted Owlet they ex-
panded. This is in tune with their known associations with forests
and open habitats, respectively. In LGM, observations of drastic veg-
etation change in Indian Peninsula from moist rainforests (Prabhu et
al., 2004; Sukumar, Suresh, & Ramesh, 1995) to tropical grasslands
(Ray & Adams, 2001) indicate that the LGM climate possibly gen-
erated habitat suitable for Spotted Owlet. The climatically suitable
areas for Jungle Owlet, however, showed a slight increase during
LGM when compared to LIG, possibly occupying a diversity of hab-
itats (moist to dry forests to scrublands). Climatically suitable areas
for the Little Owl showed a southward shift during the LGM and a
postglacial northward expansion (Figure 2, Supporting Information
Appendix S1: Figure S1.5.). Climatically suitable areas for Little
Owl during the LGM were not restricted to the European Southern
Refugia, but widespread occupying a larger area than previously
thought. Our results lend support to the Pellegrino et al., (2014) hy-
pothesis of southward range shift of the Little Owl during the LGM.
The expansion in climatically suitable areas for Forest Owlet,
during the MDH, could be due to prevailing climatic conditions
that were comparable to LIG and when woodlands were wide-
spread. In the case of Jungle Owlet, climatically suitable areas
increased during the MDH and spread into the Western Ghats,
overlapping with suitable areas for the other owlets. There is
increasing evidence supporting multiple warm and cold climate
cycles (Chauhan, 2002; Gupta, Anderson, & Overpeck, 2003;
Randhawa, 1945; Sukumar, Ramesh, Pant, & Rajagopalan, 1993)
and aridification (Ponton et al., 2012) in the tropics during the
Holocene. In Early Holocene, there is evidence of changing veg-
etation in the Western Ghats (Kumaran et al., 2014; Srivastava,
KOPARDE et al. |
      7

F I G U R E 3   The species‐wise arrangement of the climatic heterogeneity values (ranges from 0—highly homogeneous to 100—highly
heterogeneous) extracted from 1,000 random points selected from climatically suitable areas of the study owlets. CUR, Current; LGM, Last
Glacial Maximum; LIG, Last Interglacial; MDH, Mid‐Holocene. * indicates that the values differ significantly (p < 0.001, one‐way ANOVA
test) from any other category

Pal, Aruche, Wani, & Sahrawat, 2015). Post‐MDH until the cur-
rent time period such short‐term climatic fluctuations might have
further impacted climatically suitable areas for the Indian owlets.
The possible climate‐mediated vegetation changes post‐MDH
and human‐mediated land‐use change postindustrialization might
have impacted forest‐associated species such as Forest Owlet and
Jungle Owlet, and open habitat associated species such as Spotted
Owlet and Little Owl differently.
Although the owlets overlap in geographic distributions, there are
few studies examining resource sharing among the species (Ishtiaq,
2000; Jathar & Rahmani, 2004; Mehta et al., 2018; Rasmussen &
Ishtiaq, 1999; Yosef, Pande, Pawashe, Kasambe, & Mitchell, 2010).
Interspecific interactions and resource use when factored into niche
models could improve predictions (Araújo & Luoto, 2007; Wisz et
al., 2013). Incorporating data on recent as well as paleoclimatic fluc-
tuations generated for time periods not covered in this study are
recommended, to obtain a more comprehensive picture of species
responses to climate change.
4.2 | Climatically suitable areas for owlets and
climatic heterogeneity
Following the hypothesis of endemic species occupying climati-
cally stable areas (Dynesius & Jansson, 2000; Jansson, 2003), over
a gradient of range extents, we expected the following pattern: the
Forest Owlet (forest‐associated species with the lowest EOO) would
occupy climatically stable areas to a greater extent across all time
periods, followed by the Jungle Owlet (associated with forest and
scrubland), Spotted Owlet (associated with open habitat and human
settlements), and Little Owl (associated with open habitat and human
settlements but with the largest EOO). Our results showed that the
predicted climatically suitable areas for all owlets were nested in
climatically stable areas but to differing degrees in various time pe-
riods. For the Forest Owlet, climatically suitable areas were located
within climatically stable areas during all four time periods, but for
the Jungle Owlet and Spotted Owlet, this was not consistent across
all time periods (Figures 3 and 4; Supporting Information Appendix
 |
8       KOPARDE et al.

F I G U R E 4   The time period‐wise arrangement of the climatic heterogeneity values (ranges from 0—highly homogeneous to 100—highly
heterogeneous) extracted from 1,000 random points selected from climatically suitable areas of the study owlets. CUR: Current; FO: Forest
Owlet; JO: Jungle Owlet; LGM: Last Glacial Maximum; LIG: Last Interglacial; LO: Little Owl; MDH: Mid‐Holocene; SO: Spotted Owlet. *
indicates that the values differ significantly (p < 0.001, one‐way ANOVA test) from any other category

S2: Table S2.4.). During the current time period, modeled suitable
areas for all the owlets are within climatically stable areas (Figures
3 and 4) unlike during the MDH. The current nested geographical
distributions of the owlets (Figure 1) could perhaps be explained by
habitat tracking, presuming that the modeled suitable areas are good
proxies for actual geographical distributions. The climate refugia for
each owlet is different and needs to be mapped and projected con-
sidering future climate change for focused and effective conserva-
tion planning (Hannah et al., 2007).
4.3 | Caveats and conclusion
There is no definitive way to empirically validate the past distribu-
tion models constructed for the study species and hence interpreta-
tions are presumptive. Nonavailability of fossil data for focal species
makes it difficult to examine the accuracy of the past distribution
models. The two central assumptions of the study are (a) climati-
cally suitable area is a proxy for the geographical area occupied
by a species and (b) the current species–climate relationships have
been maintained in the past. We recommend validating the past
distribution models with the help of fossil occurrence data whenever
available. Apart from these major issues, the quality and accuracy of
the predictor dataset and its projections are of concern (reviewed in
Nogués‐Bravo, 2009).
Our results suggest that Quaternary climatic fluctuations might
have played a significant role in shaping the present distribution of
owlets. Such information can help in deciphering the biogeography
of species, with varying habitat associations albeit with overlapping
geographical distributions. Future research in this area should focus
on more substantial datasets incorporating information on interspe-
cific interactions and regional climate to understand the effect of
Holocene climatic fluctuations on species.
AC K N OW L E D G M E N T S
This work was supported by Department of Biotechnology,
Government of India grant (grant no. BT/PR4812/BCE/8/898/2012)
awarded to Shomita Mukherjee (S.M.), Intramural grant of Indian
Institute of Science Education and Research (IISER) Tirupati
to VV Robin (V.V.R.), and Ministry of Environment, Forest and
KOPARDE et al.
Climate Change (MoEFCC), Government of India (sanction no.
J.22012/61/2009‐CS (W), 29 September 2017) to SM & VVR. We
would like to thank State Forest Departments (Maharashtra, Madhya
Pradesh, Gujarat, and Chhattisgarh) for providing permits to collect
data on owls. Pankaj Koparde (P.K.) would like to thank the Ecology
Lab members at IISER Tirupati for discussions.
C O N FL I C T O F I N T E R E S T
None declared.
AU T H O R C O N T R I B U T I O N S
P.K., V.V.R., and S.M conceived the ideas; P.K. and P.M. collected the
data; P.K. analyzed the data; and P.K., V.V.R., and S.M. led the writing.
DATA ACC E S S I B I L I T Y
The climatic niche model output raster files can be accessed from
Data Dryad Repository https://doi.org/10.5061/dryad.9fp97gk.
ORCID
Pankaj Koparde  https://orcid.org/0000-0002-7418-8814
Prachi Mehta  https://orcid.org/0000-0002-3142-6229
Shomita Mukherjee  https://orcid.org/0000-0001-5200-8213
V. V. Robin  https://orcid.org/0000-0003-3109-5498
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S U P P O R T I N G I N FO R M AT I O N
Additional supporting information may be found online in the
Supporting Information section at the end of the article.  
How to cite this article: Koparde P, Mehta P, Mukherjee S,
Robin VV. Quaternary climatic fluctuations and resulting
climatically suitable areas for Eurasian owlets. Ecol Evol.
2019;00:1–11. https://doi.org/10.1002/ece3.5086